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& Neuroscience, 2012, 5, 2, 183 - 190 DOI: 10.3922/j.psns.2012.2.08

Neuropsychological assessment of in traumatic injury: hot and cold components Rochele Paz Fonseca, Nicolle Zimmermann, Charles Cotrena, Caroline Cardoso, Christian Haag Kristensen, and Rodrigo Grassi-Oliveira Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre, RS, Brazil

Abstract The present study compared decision-making processing between patients with (TBI) and healthy controls. The study also sought to identify dissociations in the frequency of deficits in executive functions (EF) tasks that mainly assess decision making (DM; hot component) and inhibition (cold component) following TBI. The sample was composed of 16 post- TBI adults aged between 18 and 68 years and 16 healthy controls matched by age and education. Decision-making was assessed with the Iowa Gambling Task (IGT), and inhibitory control was assessed with the Trail Making Task (TMT) and Hayling Test. No differences were found between groups in total scores and block scores on the IGT. However, TBI patients preferred the disadvantageous decks, with no evidence of during the task. Seven patients presented dissociations between deficient DM on the IGT and accurate inhibition on the Hayling Test and TMT. Conversely, five patients presented partial dissociations between deficits in the IGT and TMT and opposite performance in the Hayling Test. Only three patients exhibited deficits on all of the instruments. These results indicate that patients can maintain comparable performance on the IGT after TBI. Therefore we found dissociations in hot and cold executive components. Keywords: neuropsychological tests; executive function; decision making; inhibition; traumatic brain injury.

Received 14 June 2012; received in revised form 31 October 2012; accepted 14 December 2012. Available online 28 December 2012.

Introduction (DM; Ardila, 2008; Brock, Rimm-Kaufman, Nathanson, Executive functions (EF) can be considered a complex & Grimm, 2009; Chan et al., 2008). umbrella process that includes several subcomponents, Neuropsychological assessment in individuals with including initiation, inhibition, cognitive flexibility, traumatic brain injury (TBI) is a common necessity at shifting, switching, planning, speed of processing, and all levels of severity of this disorder because cognitive decision making, that work together to accomplishment deficits are highly prevalent during its acute and chronic phases (Fork, Bartels, Ebert, Grubich, Synowitz, & goals (Chan, Shum, Toulopoulou, & Chen, 2008; Wallesch, 2005; Zgaljardic & Temple, 2010). Initially, Verdejo-García & Bechara, 2010). In , linguistic and mnemonic assessments predominate EF has received much because of its complexity because aphasic and amnesic symptoms are more and multifactorial features, although its nature and the prominent. However, returning to work and daily components that integrate this mental function are still demands can require more detailed assessments of controversial (Elliott, 2003; Tirapu-Ustárroz, Garcia- attention and EF, which are essential for accomplishing Molina, Luna-Lario, Roig-Rovira, & Pelegrin-Valero, tasks (Clune-Ryberg et al., 2011). Neuropsychological 2008). Some authors have proposed that EF can be assessment and interventions are challenging in divided into “cold” and “hot” processes. Cold components individuals with TBI because they are influenced by are considered to demand greater use of rationality and emotional and psychiatric characteristics that can be logic, such as reasoning, and planning. Hot components present either before or after the injury (Taylor, Kreutzer, are those that involve emotion, such as decision making Demm, & Meade, 2010). Assessing the various facets of EF is relevant for rehabilitation (Milders, Ietswaart, Rochele Paz Fonseca, Nicolle Zimmermann, Charles Cotrena, Crawford, & Currie, 2008), but very little is known Caroline Cardoso, Christian Haag Kristensen and Rodrigo about hot and cold EF in this clinical population. Grassi-Oliveira, Programa de Pós-Graduação em Psicologia, Among EFs, DM processes have been studied Faculdade de Psicologia, Pontifícia Universidade Católica do in neurological patients, including TBI patients, and Rio Grande do Sul – PUC-RS. Correspondence regarding this article should be directed to: Rochele Paz Fonseca, Pontifícia psychiatric patients, such as substance abusers (Bechara Universidade Católica do Rio Grande do Sul – PUC-RS, Av. & Damásio, 2002). Decision-making has been considered Ipiranga, 6681, Partenon, Porto Alegre, RS, Brazil. Phone: 55 a hot EF that involves emotional processing (Bechara, 51 3320-3500 ramal: 7742. E-mail: [email protected] Tranel, Damásio, & Damásio, 1996; Chan et al., 2008; 184 Fonseca et al.

Happaney, Zelazo, & Stuss, 2004). Neuropsychological TBI patients and healthy controls using the IGT, the research has investigated DM processing based on TMT, and a Go-No-Go task, among other paradigms. the somatic marker hypothesis (Damásio, 1996). This Impairments in both inhibitory control and DM were theory proposes that when a person needs to make a found in TBI patients compared with controls. Levine et decision, he experiences somatic sensations (i.e., somatic al. (2005) performed a study with 71 TBI patients who markers) that occur in advance of real consequences of were assessed using the IGT and TMT and exhibited possible different alternatives. Those implicit markers impaired performance on both instruments. Although act as emotional biocatalysts of DM, in which distinct these studies investigated both DM and inhibition alternatives are evaluated emotionally, based on somatic components, to our knowledge, no studies have assessed sensations that guide adaptive DM (Damásio, 1996). DM and verbal and visuospatial inhibition using, for The ventromedial and its limbic system example, a paradigm like the Hayling Test. connections are considered key structures in the DM Because the relationships between hot and cold process (Bechara et al., 1996). The Iowa Gambling Task EF, specifically between predominant verbal and visual (IGT; Bechara, Damásio, Damásio, & Anderson, 1994; inhibition and DM, have not been investigated post- Bechara, 2007) is one of the most valued instruments TBI, the present study compared performance on the internationally for measuring emotion-based DM IGT between TBI patients and healthy controls. We also (Bowman, Evans, & Turnbull, 2005). verified the frequency of inhibition and DM deficits, Studies on DM in neurological populations have seeking to determine possible dissociations between been conducted. The IGT has been considered sensitive these EF components. to aspects of executive dysfunction after TBI (Bonatti et al., 2008; Hanten et al., 2006; Levine, Black, Cheung, Methods Campbell, O’Toole, & Schwartz, 2005; MacPherson, Phillips, Della Sala, & Cantagallo, 2009; Wiederkehr, Participants Barat, Dehail, de Seze, Lozes-Boudillon, & Giroire, 2005). Eighteen adults (12 men and four women), aged 18 Another executive component that is frequently to 68 years, who had suffered a closed TBI were recruited impaired in TBI patients compared with healthy controls through outpatient records from hospitals in Porto is inhibition (Dimoska-Di Marco, McDonald, Kelly, Tate, Alegre, Rio Grande do Sul, Brazil. Participants were & Johnstone, 2011; Felmingham, Baguley, & Green, included in the study if they did not present moderate to 2004; Perlstein, Larson, Dotson, & Kelly, 2006; Larson, severe aphasia, did not have less than 2 years of formal Kaufman, Schmalfuss, & Perlstein, 2007). Inhibition is an education, and did not have previous neurological or non- important executive ability that allows the individual to corrected sensorial disorders. All of the patients were suppress, interrupt, or delay a usual or automatic behavior native Brazilian Portuguese speakers. Two participants in favor of more complex and controlled processing were excluded because they did not complete the battery (Aron, Robbins, & Poldrack, 2004). Studies suggest that of tests, resulting in a final sample of 16 TBI patients. A TBI patients can present impairment in this EF (Rao previous history of the presence or absence of psychiatric & Lyketsos, 2000; Dimoska-Di Marco et al., 2011). disorders was not considered an exclusion criterion but The literature indicates that some neuropsychological instead was characterized as present or absent based tools, such as bipartite paradigms, are recognized for on a clinical interview. The sociocultural, individual, their ability to accurately assess inhibition because and clinical characteristics of the clinical group are they usually require more automatic processes during presented in Table 1. Neuropsychological assessment the initial phase of assessment. During later phases, was performed at least 1 month post-injury, and the time a similar paradigm is used with some differences, post-TBI varied from 1 to 50 months. requiring more controlled processing. The Trail Making The control group consisted of 16 non-brain- Test (TMT; War Department, 1944; Sánchez-Cubillo damaged adults who were matched by age and et al., 2009) and Hayling Test (Burgess & Shallice, education. A t-test indicated that the groups did not 1997; Chan et al., 2008) are frequently administered for differ from each other with regard to age (p = .370) and such a purpose. Draper & Ponsford (2008) studied 60 years of education (p = .166). A convenience sample of TBI patients who presented impaired performance on adults was recruited from workplaces and community the Hayling Test compared with controls. Periàñez et centers. The inclusion criteria for the control group al. (2007) administered the TMT to evaluate inhibitory included the absence of a history of psychiatric or control, and they also observed lower performance in TBI neurological disorders, the absence of non-corrected patients compared with healthy controls. This evidence sensorial deficits, and the non-usage of anticonvulsive, suggests that these tests are useful for diagnosing antipsychotic, and medications. impaired inhibition in TBI patients. All of the data presented in Table 1 were obtained The few studies that have investigated DM and by means of self-report through a sociocultural and cold EF components in TBI patients have suggested a medical history questionnaire (Fonseca, Oliveira, Gindri, synergic impaired profile (Levine et al., 2005; Bonatti Zimmermann, & Reppold, 2012). More specifically, et al., 2008; Sigurdardottir, Jerstad, Andelic, Roe, & this questionnaire included questions about gender, age, Schanke, 2010). Bonatti et al. (2008) assessed acute education, socioeconomic status, frequency of reading and Neuropsychological assessment of executive functions 185

Table 1. Demographic and clinical data of the TBI and control groups

TBI group Control group Variables/Groups M SD M SD Age (years) 37.31 13.65 32.88 13.09 Education (years) 10.50 3.48 12.44 4.2 Reading and writing habits 7.94 5.15 14.25 4.52 Socioeconomic score 23.44 6.87 26.63 4.89 Frequency n (%) n (%) Sex Male 12 (75.0) 9 (56.3) Demographic Data Female 4 (25.0) 7 (43.8) Handedness Right 13 (81.3) 16 (100.0) Left 3 (18.8) – M SD M SD MMSE 24.3 3.82 28.87 1.36 Frequency n (%) n (%) Severity Mild 6 (37.5) – Severe 10 (62.5) – Cause of injury Motor vehicle 8 (50.0) –

Clinical Data Fall 5 (31.25) – Sports 1 (6.25) – Others 1 (6.25) – Not specified 1 (6.25) – Previous psychiatric disorders Absence 9 (64.28) 0 (0.0) Presence 5 (35.71) 0 (0.0)

MMSE, Mini Mental State Examination. writing habits, and handedness. The frequency of reading Iowa Gambling Task (Bechara et al., 1994; Bechara, and writing habits was ranked from 0 (“I never read”) to 4 2007). A computer-based IGT version adapted to the (“I read everyday”) for books, magazines, and so on, with a southern Brazilian population by Schneider & Parente maximum score of 16, and from 0 (“I never write”) to 4 (“I (2006) was used. This version of the IGT showed write every day”) for letters, messages, and so on, with a evidence of reliability in a Brazilian sample (Cardoso, maximum score of 12 (Pawlowsky, Remor, Parente, Salles, Carvalho, Contrena, Schneider-Bakos, Kristensen, & Fonseca, & Bandeira, 2012). Additionally, handedness was Fonseca, 2010). In the IGT, the examinee chooses cards verified by means of the adapted Edinburgh Inventory with from four decks (A, B, C, and D) in 100 trials. Each a maximum score of 20. card results in either a gain or loss of money. From the four decks, two are advantageous (C and D), resulting in Procedures and instruments money gained with low monetary loss during the trial. All of the participants were assessed in a clinical The other two decks (A and B) are disadvantageous, setting in silent and ventilated rooms. They signed resulting in short-term greater gains but more frequent consent forms approved by the Ethics Committee of the losses. The task emphasizes the learning of reward university (protocol no. 10/05143 and 1679-09). They and punishment associations and is an international were assessed in two different randomized orders using reference for DM assessment (Bechara et al., 1994; the following neuropsychological instruments: Schneider-Bakos, Denburg, Fonseca, & Parente, 2010). 186 Fonseca et al.

The main dependent variables derived from the IGT are 11.95) and control group (M = -3.50, SD = 25.67). A high total score and net score ([C + D] - [A + B]) and block standard deviation was observed in both groups, mainly score ([C + D] - [A + B]) for each segment or block in controls, which might reflect the heterogeneity of the of 20 cards, frequency of deck choices, and spared or sample. The groups were also compared with regard to impaired performance according to a cut-off point of their performance in each block of 20 cards (Table 2). -10 (established by Bechara, Damasio, & Damasio, Figure 1 shows the learning curve of each group. 2000) especially in brain-damaged subjects. Table 2 shows no significant differences when each Trail Making Test (War Department, 1944). block was analyzed separately. Additionally, the data This instrument consists of two parts. In Part A, the presented in Figure 1 show no differences between participants must connect numbers randomly distributed groups with regard to their performance during the IGT on an A4 sheet of paper. In Part B, numbers and letters are blocks (p = .446; mixed ANOVA). Figure 2 presents to be alternately connected, and they are also distributed the frequency of group preferences for each of the four in a random order on an A4 sheet of paper. The number decks (A, B, C, or D). Such an analysis determines of correct answers and errors are considered, such that whether the most risky decks (A and B) or advantageous the maximum number of correct answers is 24, with decks (C and D) were chosen. no maximum number of errors. The time necessary Figure 2 suggests that the TBI group chose more to complete each part and the relationship between risky decks (A and B), whereas controls more frequently the time necessary to complete Parts B and A are also preferred cards from decks B and D. A significant analyzed. In this task, planning and processing speed difference was found between groups in deck A (p < components related to visual, perceptual, and motor .001), with TBI patients choosing this risky deck more skills (Parts A and B) and inhibition and switching (Part frequently (t-test). Table 3 shows the groups’ inhibition B) are assessed. task performance. Hayling Test (Burgess & Shallice, 1997; adapted by in measures of processing speed related to the Fonseca et al., 2010). This task consists of phrases in inhibitory process (time in Part B minus time in Part A which the last word is missing. The participants must of the Hayling Test), in which TBI patients were slower complete it with a word that properly fits the sentence than controls. The errors variable of the TMT, Part B, (Part A; completing the sentence normally) and with was significantly different between groups, with inferior an unrelated word (Part B). Time and accuracy are performance in TBI patients. measured, with a maximum of 15 for quantitative scoring When analyzed together, the Z scores of deficits and a maximum of 45 for quantitative-qualitative errors in tasks of hot and cold EF showed that seven patients on Part B. Initiation (Part A), verbal inhibition (Part B), presented dissociations in performance on the IGT and processing speed (i.e., both parts and relationship (i.e., deficits) and normal performance on the TMT between time for Part B and Part A) components are and Hayling Test. Five subjects presented deficient assessed. performance on the IGT and TMT and normal performance on the Hayling Test. The greater frequency Statistical analysis of patients with impaired DM may be associated with a All of the descriptive and inferential analyses were greater frequency of severe TBI patients in the clinical performed using the Statistical Package for the Social group; therefore, an additional analysis was conducted. Sciences (SPSS 17.0). A normal distribution was observed No differences were found between mild and severe in both groups according to the Kolmogorov-Smirnov Test. subgroups of TBI patients with regard to the frequency Mean comparisons between the TBI and control groups of deficits on the IGT, Hayling Test, and TMT (Fisher’s were conducted using an independent samples t-test for Exact Test, p > .05). the DM variables (i.e., IGT total and block scores) and inhibition variables (i.e., Hayling Test and Trail Making Table 2. Performance of each group in Iowa Gambling Task Test accuracy and time). To compare performance in each blocks block of the IGT between groups during the five segments, M (SD) t p value a mixed analysis of variance (ANOVA) was performed. To Block 1 TBI -3.63 (5.62) -.227 .82 investigate possible dissociations between the occurrence Controls -3.13 (6.81) of deficits in DM and other cold EFs, the Z score was calculated for the variables in the Hayling Test and Trail Block 2 TBI .38 (6.24) -.056 .95 Making Test. The participants were also classified on the Controls .50 (6.42) IGT as having non-impaired or impaired DM abilities Block 3 TBI -.50 (3.05) -.640 .53 based on the cut-off scores established by Bechara, Controls 1.13 (9.68) Damasio, & Damasio (2000). Block 4 TBI 0.00 (3.09) .984 .33 Results Controls -2.88 (11.26) Block 5 TBI -1.13 (3.79) -.863 .39 No difference was found in IGT total score (p = .638; t-test) between the TBI group (M = -6.88, SD = Controls .88 (8.45) Neuropsychological assessment of executive functions 187

5

4

3

2

1 TBI group 0

–1 1 234 5 Control group

Mean of block score –2

–3

–4

–5 Blocks

Figure 1. Group performance during the blocks on the Iowa Gambling Task.

100

35.38 28.5 28.69 25.06 23.19 23.5 20.31 17.13

10 TBI group

Control group

Number of choices per deck

1 A BCD Decks Figure 2. Group preferences for each of the four decks in the Iowa Gambling Task.

Discussion When interpreted together, these findings suggest The present results suggest that the TBI patients’ that despite nonsignificant differences between groups global performance on the IGT, as a group, did not differ in total score, TBI patients presented more risk-taking from DM processing in healthy controls. Although no behavior. Van Noordt & Good (2011) also did not find difference was found in the block score, a greater peak differences between controls and mild TBI patients on of learning was observed in healthy controls. Despite self-reports. However, injury severity was inversely the fact that the control group changed its performance related to DM performance, such that as injury status in Block 4, these participants may have preferred increased, the quality of this EF processing decreased. more risky cards, looking to gain more money during These authors pointed out the great heterogeneity this segment of the task. In the TBI group, observing of cognitive deficits after mild TBI. In this context, a learning curve was not possible during the task, but such findings can partially explain the results of the a constant curve was observed from Block 2 to Block present study with regard to the absence of significant 5. Conversely, in a previous study, healthy individuals differences between groups in total and block scores. initiated the selection of advantageous decks from Nevertheless, we highlight the preference of the TBI 30 cards onward, whereas clinical samples generally group for the disadvantageous deck (A), which might showed an inability to choose advantageous decks be associated with the prevalence of 62.5% of severe (Dunn, Dalgleish, & Lawrence, 2006). In the present TBI in the sample. study, TBI patients preferred disadvantageous decks (A Our findings are generally corroborated by other and B), followed by a significant difference between investigations that evaluated DM in TBI patients using groups in deck A. the IGT, in which impaired performance was found 188 Fonseca et al.

Table 3. Performance of groups in TMT and Hayling Test

Tasks/variables Groups M SD F p

Time B/time A TBI 4.42 4.08 3.120 .099 Controls 2.64 .93 Qualitative errors Part B (/45) TBI 19.00 10.18 .249 .054 Controls 12.19 8.98 Correct answers Part A (/15) TBI 14.69 .60 .789 .741 Controls 14.75 .45 Errors Part A (/15) TBI .31 .60 2.248 .495 Controls .19 .40

Hayling Test Correct answers Part B (/15) TBI 7.44 3.18 .011 .088 Controls 9.60 3.64 Errors Part B (/15) TBI 7.88 3.05 .158 .067 Controls 5.63 3.63 Time Part B - Time Part A TBI 61.93 52.16 6.531 .018 Controls 26.22 17.98 Errors Part A TBI .13 .34 1.454 .559 Controls 0.06 .25 Correct answers Part B (/24) TBI 22.69 3.11 15.026 .112 Controls 24.00 0.00 Time Part B - Time Part A / Time Part A TBI 2.00 1.66 .813 .457 Controls 1.56 1.50 Time Part B / Time Part A TBI 3.26 1.66

Trail Making Test Trail 1.843 .218 Controls 2.56 1.50 Errors Part B TBI 3.63 4.43 19.980 .017 Controls .63 .81 compared with controls (García-Molina, Roig-Rovira, Therefore, although not a direct aim of this study, our Enseñat-Cantallops, Sánchez-Carrión, Pico-Azanza, & findings suggest that even with a reduced sample of 16 Pena-Casanova, 2007). In these studies, TBI patients patients, a tendency toward deficits was observed in the failed to learn during five blocks of the IGT. These TBI group compared with healthy controls, independent data characterize a failure in DM processing based on of the lesion site. These studies suggest that our results the somatic marker hypothesis assessed by the task might not be specifically related to frontal damage. (Bonatti et al., 2008; Sigurdardottir et al., 2010). Figure Dissociations between deficits have important 1 shows that the TBI group did not present typical implications for both theoretical and clinical fields. The learning, although no significant differences were found first dissociation (i.e., patients had impaired performance in the mixed ANOVA. This might be attributable to the on the IGT and normal performance on the TMT and groups’ sample sizes. With the exception of one TBI Hayling Test) might be explained in terms of distinct hot patient, other patients were impaired in the task. This and cold components of EF. The dissociation between finding is consistent with previous studies (Levine et al., the two inhibition assessment tasks may be explained by 2005; Sigurdardottir et al., 2010). We hypothesize that dissociations between verbal and non-verbal inhibitory dissociations may exist between groups, depending on ability, which require different demands on the the severity of trauma and sample size. executive system. Three patients presented deficits in all In studies that controlled the lesion site in TBI, of the tasks in the present study, showing impaired hot performance appeared to be influenced by lesions that and cold EF. This may be explained by previous studies affected neural circuitry involved in DM processing. that found associations between DM and inhibitory However, recent investigations indicated that lesions control deficits assessed by both the IGT and TMT that do not involve the prefrontal ventromedial cortex (Bonatti et al., 2008; Levine et al., 2005) and studies of (MacPherson et al., 2009) or frontal cortex (Levine et inhibitory control that assessed verbal and non-verbal al., 2005) are associated with impaired performance inputs using the Hayling Test (Draper & Ponsford, on this instrument. Our sample was composed of four 2008) and TMT (Periàñez et al., 2007), respectively. patients with lesions exclusively in the frontal lobes and Only one mild TBI patient did not present deficits in other areas, four patients with lesions exclusively in the any task. We emphasize the heterogeneity of mild TBI frontal lobe, four patients with lesions in other brain neuropsychological deficits (37.5% of our sample). Our areas, and four patients with no diagnosed brain damage. results are generally consistent with studies that showed Neuropsychological assessment of executive functions 189 distinct impairments in EF in TBI patients (Dimoska-Di Cardoso, O.C., Carvalho, J.C.N., Cotrena, C., Schneider-Bakos, D.G., Marco et al., 2011; Felmingham et al., 2004; Perlstein et Kristensen, H.C., & Fonseca, R.P. (2010). Estudo de fidedignidade do instrumento neuropsicológico Iowa Gambling Task. Jornal al., 2006; Larson et al., 2007). Brasileiro de Psiquiatria, 59(4), 279-285. 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